Acacia trees pass on an ‘alarm signal’ to other trees when antelope browse on their leaves, according to a zoologist from Pretoria University. Wouter Van Hoven says that acacias nibbled by antelope produce leaf tannin in quantities lethal to the browsers, and emit ethylene into the air which can travel up to 50 yards. The ethylene warns other trees of the impending danger, which then step up their own production of leaf tannin within just five to ten minutes.

Van Hoven made his discovery when asked to investigate the sudden death of some 3000 South African antelope, called kudu, on game ranches in the Transvaal. He noticed that giraffe, roaming freely, browsed only on one acacia tree in ten, avoiding those trees which were downwind. Kudu, which are fenced in on the game ranches, have little other than acacia leaves to eat during the winter months. So the antelope continue to browse until the tannin from the leaves sets off a lethal metabolic chain reaction in their bodies.

Van Hoven’s research is to be published in the Journal of African Zoology. He described his results at a recent conference in France. Claude Edelin of the National Scientific Research Centre (CNRS) described the discovery as ‘terribly exciting’. Fifteen years ago, a French scientist at the CNRS, Paul Caro, found that oak trees attacked by caterpillars reacted by stepping up the quantity of tannin and phenol produced in their leaves. Caro observed that the trees’ defence mechanism inhibited the growth of the larvae.

At first it may seem counter-intuitive: that preventing large African herbivores from browsing Acacia trees decreases their growth. This, however, is precisely what researchers report in Science magazine. It is all because of the Acacia’s mutually beneficial relationship with a biting ant. Together they fend off Africa’s big grazing mammals; but it is these very antagonists that are needed to keep the plant-insect team working in concert. “Simulating large mammal extinction, by experimentally excluding them from eating the trees, causes the ant-plant mutualism to break down,” said co-author Robert Pringle from Stanford University, US. The whistling thorn tree (Acacia drepanolobium) and the biting ant (Crematogaster) that lives on it form a relationship, evolved over many millennia, in which both species co-operate and in turn benefit from each other.

Ant bodyguards
When this “mutualism” is working well, Acacia trees provide ants with swollen thorns, which serve as nesting sites; and nectar, which the ants collect from the bases of Acacia leaves. In return for this investment, ants protect the tree from browsing mammals by aggressively swarming against anything that disturbs the tree. Mr Pringle explains: “It is as if the tree hires bodyguards, in the form of ants, to protect it from being eaten.” The researchers disrupted this relationship by fencing off six plots of savanna land in Kenya by an 8,000-volt electric fence for 10 years.

Herbivores, such as giraffes and elephants, were no longer able to feed on the trees, causing a change in plant-ant dynamics. “[The trees] diminish the rewards that they produce for the ant bodyguards, decreasing both the amount of housing and the amount of sugar-rich nectar they produce,” lead-author Dr Todd Palmer at the University of Florida, US, told the BBC News website. He continued: “In essence, the trees begin to default on the co-operative bargain that they’ve made with the ants, because the trees no longer have need for protection from large browsing mammals like giraffes and elephants.” It would seem that now the trees are better off, as they do not need to use their resources to support the ants – but the researchers have revealed that this is not the case. Due to lack of housing and food, the mutualistic ant species becomes less aggressive, its colony size decreases and it loses its competitive edge.

Conservation implications
“The net result is a community-wide replacement of the ‘good’ mutualist ant by a decidedly ‘bad’ ant species that does not protect the trees from herbivores, and actually helps a wood-boring beetle to create tunnels throughout the main stem and branches of the acacia trees, which the bad ant then uses as nesting space,” Dr Palmer explains. Trees occupied by this antagonist ant grow more slowly and experience double the death rate compared with trees occupied by the mutalistic ant. At present, the researchers do not fully understand the mechanisms that allow the tree to sense it is no longer being browsed and to turn off its investment in mutualistic ants, but they suggest it takes place over a 5-10-year period. Dr Palmer said there were two important conservation implications of this research: “The first is that the decline of these charismatic [large animals] can have complex and cascading effects on entire ecosystems, with unanticipated results. “The second is that classical conservation approaches talk about conserving species, but perhaps equally important is the conservation of ‘interactions’.” The researchers suggest that the loss of large herbivores throughout Africa, due to ongoing human activity, may have strong and unanticipated consequences on the broader community. Mr Pringle adds: “It is a cautionary tale.”

In Africa and in the tropics, armies of tiny creatures make the twisting stems of acacia plants their homes. Aggressive, stinging ants feed on the sugary nectar the plant provides and live in nests protected by its thick bark. This is the world of “ant guards”. The acacias might appear overrun by them, but the plants have the ants wrapped around their little stems. These same plants that provide shelter and produce nourishing nectar to feed the insects also make chemicals that send them into a defensive frenzy, forcing them into retreat.

Nigel Raine, a scientist working at Royal Holloway, University of London in the UK has studied this plant-ant relationship. Dr Raine and his colleagues from the universities of St Andrews, Edinburgh and Reading in the UK and Lund University in Sweden have been trying to work out some of the ways in which the insects and the acacias might have co-evolved. He explains how the ants provide a useful service for the acacias. “They guard the plants they live on,” said Dr Raine. “If other animals try to come and feed on the rich, sugary nectar, they will attack them.”

In Africa, one type of ant-guard, known as Crematogaster, will even attack large herbivores that attempt to eat the plant. “If a giraffe starts to eat the leaves of an acacia that is inhabited by ants, the ants will come out and swarm on to its face, biting and stinging,” says Dr Raine. “Eventually, the giraffe will get fed up and move off.” In the New World tropics, the Pseudomyrmex genus of ants fulfil a very similar guarding role. For both species, the acacias provide little, reinforced structures that the ants hollow out and nest within, as well as sugar-rich nectar for them to eat. “In return, both groups of ants protect their host plants from herbivores – both hungry insects and larger [animals],” explains Dr Raine.

Give and take
That is the plus side for the plants. But being inhabited by aggressive insects could make one important aspect of a plant’s life difficult – flowering. Flowers need to be pollinated so the plant can reproduce. So what stops the ants from attacking the helpful little pollinators or stealing all the tasty nectar that attracts them? “Some plants do this structurally, with physical barriers to stop ants getting on to the flower, or sticky or slippery surfaces that the insects can’t walk on,” said Dr Raine. “Acacias don’t have these barriers. They have very open flowers, but still, the ants don’t seem to go on to them. We wanted to know why.”

One clever approach by the plant is a food “bribe”. “Extrafloral nectaries” are small stores of nectar on stems, from which the inhabitants can feed without going on to the flowers. Acacias also produce structures called beltian bodies on the leaf tips. These, Dr Raine explains, are nutritious structures produced by the plant to feed its resident colony of ant-guards. But when this isn’t enough, it is a case of chemical warfare. Flowers can produce a variety of chemicals. We can smell some of the volatile organic compounds they release when we sniff our favourite summer bloom. But there is a more manipulative side to these scents. Floral volatile compounds can act as signals – drawing in pollinators such as bees and hummingbirds in with their irresistible aromas.

To the ants, however, they are far from irresistible. “The flowers seem to produce chemicals that are repellent to the ants,” said Dr Raine. “They release these particularly during the time when they’re producing lots of pollen, so the ants are kept off the flowers.” In recent studies, described in the journal Functional Ecology, Dr Raine and his colleagues found that the plants with the closest relationships with ants – those that provided homes for their miniature guard army – produced the chemicals that were most effective at keeping the ants at bay. “And that was associated with the flower being open,” he says. “So the chemicals are probably in the pollen.”

When the pollen has all been taken away – by being brushed on to the bodies of hungry pollinators and helpfully delivered to other plants – the flowers become less repellent. “So at this point, the ants can come on to the flowers and can protect them from other insects that might eat them, so that the developing seeds aren’t lost,” he explains. Dr Raines’ team was able to test this using young flowers that had just opened and that contained lots of pollen. The scientists wiped them on older flowers and on the acacia’s stems. This showed them that the effect was “transferrable” – the stems and older flowers that had been wiped became more repellent. “It gives this really neat feedback system – the plant is protected when it needs to be protected, but not when it doesn’t.”

Selective deterrents
The repellent chemicals are specific to the ants. In fact, they attract and repel different groups of insects. “[The chemicals] don’t repel bees, even though they are quite closely related to ants. And in some cases, the chemicals actually seem to attract the bees,” says Dr Raine. The researchers think that some of the repellents that acacias produce are chemical “mimics” of signalling pheromones that the ants use to communicate. “We put flowers into syringes and puffed the scent over the ant to see how they would respond, and they became quite agitated and aggressive” he explained. “The ants use a pheromone to signal danger; if they’re being attacked by a bird they will release that chemical that will quickly tell the other ants to retreat.” Dr Raine says this clever evolutionary system shows how the ants and their plants have evolved to protect, control and manipulate each other. The ants may be quick to swarm, bite and sting, but the harmless-looking acacias have remained one step ahead.